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Columnar distribution of activity dependent gabaergic depolarization in sensorimotor cortical neurons

BACKGROUND: GABA, the major inhibitory neurotransmitter in CNS, has been demonstrated to paradoxically produce excitation even in mature brain. However activity-dependent form of GABA excitation in cortical neurons has not been observed. Here we report that after an intense electrical stimulation ad...

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Autores principales: Lee, Jaekwang, Woo, Junsung, Favorov, Oleg V, Tommerdahl, Mark, Lee, C Justin, Whitsel, Barry L
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2012
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3520830/
https://www.ncbi.nlm.nih.gov/pubmed/23006518
http://dx.doi.org/10.1186/1756-6606-5-33
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author Lee, Jaekwang
Woo, Junsung
Favorov, Oleg V
Tommerdahl, Mark
Lee, C Justin
Whitsel, Barry L
author_facet Lee, Jaekwang
Woo, Junsung
Favorov, Oleg V
Tommerdahl, Mark
Lee, C Justin
Whitsel, Barry L
author_sort Lee, Jaekwang
collection PubMed
description BACKGROUND: GABA, the major inhibitory neurotransmitter in CNS, has been demonstrated to paradoxically produce excitation even in mature brain. However activity-dependent form of GABA excitation in cortical neurons has not been observed. Here we report that after an intense electrical stimulation adult cortical neurons displayed a transient GABA excitation that lasted for about 30s. RESULTS: Whole-cell patch recordings were performed to evaluate the effects of briefly applied GABA on pyramidal neurons in adult rodent sensorimotor cortical slice before and after 1 s, 20 Hz suprathreshold electrical stimulation of the junction between layer 6 and the underlying white matter (L6/WM stimulation). Immediately after L6/WM stimulation, GABA puffs produced neuronal depolarization in the center of the column-shaped region. However, both prior to or 30s after stimulation GABA puffs produced hyperpolarization of neurons. 2-photon imaging in neurons infected with adenovirus carrying a chloride sensor Clomeleon revealed that GABA induced depolarization is due to an increase in [Cl(-)](i) after stimulation. To reveal the spatial extent of excitatory action of GABA, isoguvacine, a GABA(A) receptors agonist, was applied right after stimulation while monitoring the intracellular Ca(2+) concentration in pyramidal neurons. Isoguvacine induced an increase in [Ca(2+)](i) in pyramidal neurons especially in the center of the column but not in the peripheral regions of the column. The global pattern of the Ca(2+) signal showed a column-shaped distribution along the stimulation site. CONCLUSION: These results demonstrate that the well-known inhibitory transmitter GABA rapidly switches from hyperpolarization to depolarization upon synaptic activity in adult somatosensory cortical neurons.
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spelling pubmed-35208302012-12-13 Columnar distribution of activity dependent gabaergic depolarization in sensorimotor cortical neurons Lee, Jaekwang Woo, Junsung Favorov, Oleg V Tommerdahl, Mark Lee, C Justin Whitsel, Barry L Mol Brain Research BACKGROUND: GABA, the major inhibitory neurotransmitter in CNS, has been demonstrated to paradoxically produce excitation even in mature brain. However activity-dependent form of GABA excitation in cortical neurons has not been observed. Here we report that after an intense electrical stimulation adult cortical neurons displayed a transient GABA excitation that lasted for about 30s. RESULTS: Whole-cell patch recordings were performed to evaluate the effects of briefly applied GABA on pyramidal neurons in adult rodent sensorimotor cortical slice before and after 1 s, 20 Hz suprathreshold electrical stimulation of the junction between layer 6 and the underlying white matter (L6/WM stimulation). Immediately after L6/WM stimulation, GABA puffs produced neuronal depolarization in the center of the column-shaped region. However, both prior to or 30s after stimulation GABA puffs produced hyperpolarization of neurons. 2-photon imaging in neurons infected with adenovirus carrying a chloride sensor Clomeleon revealed that GABA induced depolarization is due to an increase in [Cl(-)](i) after stimulation. To reveal the spatial extent of excitatory action of GABA, isoguvacine, a GABA(A) receptors agonist, was applied right after stimulation while monitoring the intracellular Ca(2+) concentration in pyramidal neurons. Isoguvacine induced an increase in [Ca(2+)](i) in pyramidal neurons especially in the center of the column but not in the peripheral regions of the column. The global pattern of the Ca(2+) signal showed a column-shaped distribution along the stimulation site. CONCLUSION: These results demonstrate that the well-known inhibitory transmitter GABA rapidly switches from hyperpolarization to depolarization upon synaptic activity in adult somatosensory cortical neurons. BioMed Central 2012-09-24 /pmc/articles/PMC3520830/ /pubmed/23006518 http://dx.doi.org/10.1186/1756-6606-5-33 Text en Copyright ©2012 Lee et al.; licensee BioMed Central Ltd. http://creativecommons.org/licenses/by/2.0 This is an Open Access article distributed under the terms of the Creative Commons Attribution License ( http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
spellingShingle Research
Lee, Jaekwang
Woo, Junsung
Favorov, Oleg V
Tommerdahl, Mark
Lee, C Justin
Whitsel, Barry L
Columnar distribution of activity dependent gabaergic depolarization in sensorimotor cortical neurons
title Columnar distribution of activity dependent gabaergic depolarization in sensorimotor cortical neurons
title_full Columnar distribution of activity dependent gabaergic depolarization in sensorimotor cortical neurons
title_fullStr Columnar distribution of activity dependent gabaergic depolarization in sensorimotor cortical neurons
title_full_unstemmed Columnar distribution of activity dependent gabaergic depolarization in sensorimotor cortical neurons
title_short Columnar distribution of activity dependent gabaergic depolarization in sensorimotor cortical neurons
title_sort columnar distribution of activity dependent gabaergic depolarization in sensorimotor cortical neurons
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3520830/
https://www.ncbi.nlm.nih.gov/pubmed/23006518
http://dx.doi.org/10.1186/1756-6606-5-33
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